Team 03: Histone variants and the nuclear envelope in heterochromatin organization

Our group is interested in the molecular mechanisms implicated in maintenance and developmental dynamics of heterochromatin organization in the model system Arabidopsis. We study heterochromatin composition in histone variants, heterochromatin position within the nucleus in respect to the nuclear envelope and the transcriptional regulation occurring at heterochromatic loci.


Historically, our laboratory was one of the pioneers in the discovery of a specific class of repeated sequences in the Arabidopsis genome, the clusters of 5S ribosomal RNA (rRNA) genes that encode a critical RNA component of the ribosome. Despite being situated within the transcriptionally repressive environment of pericentromeric heterochromatin, part of the 5S rRNA genes is highly transcribed. Our work showed that 5S rRNA expression is controlled through the availability of its specific transcription factor TFIIIA, and epigenetic mechanisms such as the RNA directed DNA methylation pathway. Together, these different modes of regulation allow fine-tuning of 5S rRNA transcription during development and overcome the repressive effect of the heterochromatic environment.

While we continue studying 5S rDNA clusters as model genes situated within heterochromatin, we now concentrate our efforts on better defining intrinsic features of heterochromatin organization and its dynamics. For that purpose we pursue two complementary approaches, which aim to identify the critical players involved in establishment and maintenance of heterochromatin in Arabidopsis:

We study histone variants and their mode of incorporation into chromatin, which is controlled by specific histone chaperone proteins. Our aim is to understand how the different variants together with their specific post-translational modifications impact heterochromatin organization and function.

We further investigate the molecular structures implicated in the nuclear-cytoplasmic crosstalk and focus on identifying complexes that link chromatin to the nuclear periphery. Indeed, the periphery of the nucleus has emerged as an anchoring point for certain chromatin domains and to impact their expression. Using reverse genetic approaches and specifically developed 3D imaging tools in collaboration with bio-mathematicians, we aim to understand the interrelationship between nuclear position, chromatin organization and gene expression. 

Research thematics


Last Name First Name Position Contact
Simon AMIARD profile picture AMIARD Simon Research Fellow
Remi CAUDRON profile picture CAUDRON Remi Intern
Sylviane COTTERELL profile picture COTTERELL Sylviane Associate Professor
Sophie DESSET profile picture DESSET Sophie Research Engineer
Tristan DUBOS profile picture DUBOS Tristan Ph.D Student
Franziska FISCHER profile picture FISCHER Franziska Assistant Engineer
Samuel LE GOFF profile picture LE GOFF Samuel Associate Professor
Aline PROBST profile picture PROBST Aline Principal Investigator
Aurelia STEVENS profile picture STEVENS Aurelia Associate Professor
Christophe TATOUT profile picture TATOUT Christophe Professor
Sylvie TUTOIS profile picture TUTOIS Sylvie Associate Professor
Emmanuel VANROBAYS profile picture VANROBAYS Emmanuel Associate Professor


  • 2018
    • S. Kemeny, C. Tatout, G. Salaun, C. Pebrel-Richard, C. Goumy, N. Ollier, E. Maurin, B. Pereira, P. Vago and L. Gouas, “Spatial organization of chromosome territories in the interphase nucleus of trisomy 21 cells.”, Chromosoma, vol. 127 (2) , pp. 247–259, 2018.
    • M. Benoit, L. Simon, S. Desset, C. Duc, S. Cotterell, A. Poulet, S. Le Goff, C. Tatout and A. Probst, “Replication-coupled histone H3.1 deposition determines nucleosome composition and heterochromatin dynamics during Arabidopsis seedling development.”, The New phytologist, 2018.
    • G. Parry, A. Probst, C. Baroux and C. Tatout, “Meeting report - INDEPTH kick-off meeting.”, Journal of cell science, vol. 131 (12) , 2018.
    • C. Charbonnel, O. Rymarenko, O. Da Ines, F. Benyahya, C. White, F. Butter and S. Amiard, “The Linker Histone GH1-HMGA1 Is Involved in Telomere Stability and DNA Damage Repair.”, Plant physiology, vol. 177 (1) , pp. 311–327, 2018.
    • L. Simon, F. Rabanal, T. Dubos, C. Oliver, D. Lauber, A. Poulet, A. Vogt, A. Mandlbauer, S. Le Goff, A. Sommer, H. Duborjal, C. Tatout and A. Probst, “Genetic and epigenetic variation in 5S ribosomal RNA genes reveals genome dynamics in Arabidopsis thaliana.”, Nucleic Acids Res., 2018.
    • A. Probst, “A Compendium of Methods to Analyze the Spatial Organization of Plant Chromatin.”, Meth. Mol. Biol., vol. 1675 , pp. 397–418, 2018.
    • L. Simon and A. Probst, “High-Affinity LNA-DNA Mixmer Probes for Detection of Chromosome-Specific Polymorphisms of 5S rDNA Repeats in Arabidopsis thaliana.”, Meth. Mol. Biol., vol. 1675 , pp. 481–491, 2018.
    • S. Desset, A. Poulet and C. Tatout, “Quantitative 3D Analysis of Nuclear Morphology and Heterochromatin Organization from Whole-Mount Plant Tissue Using NucleusJ.”, Meth. Mol. Biol., vol. 1675 , pp. 615–632, 2018.
    • A. Poulet, X. Zhou, K. Tamura, I. Meier, C. Tatout, K. Graumann and D. Evans, “Computational Methods for Studying the Plant Nucleus.”, Meth. Mol. Biol., vol. 1840 , pp. 205–219, 2018.
    • M. Voisin, E. Vanrobays and C. Tatout, “Investigation of Nuclear Periphery Protein Interactions in Plants Using the Membrane Yeast Two-Hybrid (MbY2H) System.”, Meth. Mol. Biol., vol. 1840 , pp. 221–235, 2018.
  • 2017
  • 2016
  • 2015
    • S. Smith, C. Galinha, S. Desset, F. Tolmie, D. Evans, C. Tatout and K. Graumann, “Marker gene tethering by nucleoporins affects gene expression in plants.”, Nucleus, vol. 6 (6) , pp. 471–8, 2015.
    • A. Probst and O. Mittelsten Scheid, “Stress-induced structural changes in plant chromatin.”, Curr. Opin. Plant Biol., vol. 27 , pp. 8–16, 2015.
    • V. Muchova, S. Amiard, I. Mozgova, M. Dvorackova, M. Gallego, C. White and J. Fajkus, “Homology-dependent repair is involved in 45S rDNA loss in plant CAF-1 mutants.”, Plant J., vol. 81 (2) , pp. 198–209, 2015.
    • C. Duc, M. Benoit, S. Goff, L. Simon, A. Poulet, S. Cotterell, C. Tatout and A. Probst, “The histone chaperone complex HIR maintains nucleosome occupancy and counterbalances impaired histone deposition in CAF-1 complex mutants.”, Plant J., 2015.
    • L. Simon, M. Voisin, C. Tatout and A. Probst, “Structure and Function of Centromeric and Pericentromeric Heterochromatin in Arabidopsis thaliana.”, Front Plant Sci, vol. 6 , pp. 1049, 2015.
    • P. Merle, M. Gueugneau, M. Teulade-Fichou, M. Muller-Barthelemy, S. Amiard, E. Chautard, C. Guetta, V. Dedieu, Y. Communal, J. Mergny, M. Gallego, C. White, P. Verrelle and A. Tchirkov, “Highly efficient radiosensitization of human glioblastoma and lung cancer cells by a G-quadruplex DNA binding compound.”, Scientific reports, vol. 5 , pp. 16255, 2015.
  • 2014
    • K. Graumann, E. Vanrobays, S. Tutois, A. Probst, D. Evans and C. Tatout, “Characterization of two distinct subfamilies of SUN-domain proteins in Arabidopsis and their interactions with the novel KASH-domain protein AtTIK.”, J. Exp. Bot., vol. 65 (22) , pp. 6499–512, 2014.
    • A. Poulet, I. Arganda-Carreras, D. Legland, A. Probst, P. Andrey and C. Tatout, “NucleusJ: an ImageJ plugin for quantifying 3D images of interphase nuclei.”, Bioinformatics (Oxford, England), 2014.
    • P. Kalhorzadeh, Z. Hu, T. Cools, S. Amiard, E. Willing, N. De Winne, K. Gevaert, G. De Jaeger, K. Schneeberger, C. White and L. De Veylder, “Arabidopsis thaliana RNase H2 deficiency counteracts the needs for the WEE1 checkpoint kinase but triggers genome instability.”, Plant Cell, vol. 26 (9) , pp. 3680–92, 2014.
    • C. Tatout, D. Evans, E. Vanrobays, A. Probst and K. Graumann, “The plant LINC complex at the nuclear envelope.”, Chromosome Res., 2014.
    • M. Thomas, L. Pingault, A. Poulet, J. Duarte, M. Throude, S. Faure, J. Pichon, E. Paux, A. Probst and C. Tatout, “Evolutionary history of Methyltransferase 1 genes in hexaploid wheat.”, BMC genomics, vol. 15 , pp. 922, 2014.
  • 2013
    • M. Casanova, M. Pasternak, F. El Marjou, P. Le Baccon, A. Probst and G. Almouzni, “Heterochromatin reorganization during early mouse development requires a single-stranded noncoding transcript.”, Cell Rep, vol. 4 (6) , pp. 1156–67, 2013.
    • M. Benoit, E. Layat, S. Tourmente and A. Probst, “Heterochromatin dynamics during developmental transitions in Arabidopsis - a focus on ribosomal DNA loci.”, Gene, vol. 526 (1) , pp. 39–45, 2013.
  • 2012
    • E. Layat, A. Probst and S. Tourmente, “Structure, function and regulation of Transcription Factor IIIA: From Xenopus to Arabidopsis.”, Biochim. Biophys. Acta, vol. 1829 (3-4) , pp. 274–82, 2012.
    • A. Ayar, S. Wehrkamp-Richter, J. Laffaire, S. Le Goff, J. Levy, S. Chaignon, H. Salmi, A. Lepicard, C. Sallaud, M. Gallego, C. White and W. Paul, “Gene targeting in maize by somatic ectopic recombination.”, Plant Biotechnol. J., vol. 11 (3) , pp. 305–14, 2012.
    • W. Wei, Z. Ba, M. Gao, Y. Wu, Y. Ma, S. Amiard, C. White, J. Rendtlew Danielsen, Y. Yang and Y. Qi, “A role for small RNAs in DNA double-strand break repair.”, Cell, vol. 149 (1) , pp. 101–12, 2012.
    • A. Poulet, S. Pisano, C. Faivre-Moskalenko, B. Pei, Y. Tauran, Z. Haftek-Terreau, F. Brunet, Y. Le Bihan, M. Ledu, F. Montel, N. Hugo, S. Amiard, F. Argoul, A. Chaboud, E. Gilson and M. Giraud-Panis, “The N-terminal domains of TRF1 and TRF2 regulate their ability to condense telomeric DNA.”, Nucleic Acids Res., vol. 40 (6) , pp. 2566–76, 2012.
  • 2011
    • G. Almouzni and A. Probst, “Heterochromatin maintenance and establishment: lessons from the mouse pericentromere.”, Nucleus, vol. 2 (5) , pp. 332–8, 2011.
    • B. Tamasloukht, M. Wong Quai Lam, Y. Martinez, K. Tozo, O. Barbier, C. Jourda, A. Jauneau, G. Borderies, S. Balzergue, J. Renou, S. Huguet, J. Martinant, C. Tatout, C. Lapierre, Y. Barriere, D. Goffner and M. Pichon, “Characterization of a cinnamoyl-CoA reductase 1 (CCR1) mutant in maize: effects on lignification, fibre development, and global gene expression.”, J. Exp. Bot., vol. 62 (11) , pp. 3837–48, 2011.
    • A. Probst and G. Almouzni, “Heterochromatin establishment in the context of genome-wide epigenetic reprogramming.”, Trends Genet., vol. 27 (5) , pp. 177–85, 2011.
    • C. Maison, D. Bailly, D. Roche, R. Montes de Oca, A. Probst, I. Vassias, F. Dingli, B. Lombard, D. Loew, J. Quivy and G. Almouzni, “SUMOylation promotes de novo targeting of HP1alpha to pericentric heterochromatin.”, Nat. Genet., vol. 43 (3) , pp. 220–7, 2011.
    • C. Maison, J. Quivy, A. Probst and G. Almouzni, “Heterochromatin at mouse pericentromeres: a model for de novo heterochromatin formation and duplication during replication.”, Cold Spring Harb. Symp. Quant. Biol., vol. 75 , pp. 155–65, 2011.
  • 2010
    • A. Probst, I. Okamoto, M. Casanova, F. El Marjou, P. Le Baccon and G. Almouzni, “A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development.”, Dev. Cell, vol. 19 (4) , pp. 625–38, 2010.
    • J. Ye, C. Lenain, S. Bauwens, A. Rizzo, A. Saint-Leger, A. Poulet, D. Benarroch, F. Magdinier, J. Morere, S. Amiard, E. Verhoeyen, S. Britton, P. Calsou, B. Salles, A. Bizard, M. Nadal, E. Salvati, L. Sabatier, Y. Wu, A. Biroccio, A. Londono-Vallejo, M. Giraud-Panis and E. Gilson, “TRF2 and apollo cooperate with topoisomerase 2alpha to protect human telomeres from replicative damage.”, Cell, vol. 142 (2) , pp. 230–42, 2010.
    • I. Ourliac-Garnier, A. Poulet, R. Charif, S. Amiard, F. Magdinier, K. Rezai, E. Gilson, M. Giraud-Panis and S. Bombard, “Platination of telomeric DNA by cisplatin disrupts recognition by TRF2 and TRF1.”, Journal of biological inorganic chemistry : JBIC : a publication of the Society of Biological Inorganic Chemistry, vol. 15 (5) , pp. 641–54, 2010.
    • E. Vanrobays, B. Jennings and D. Ish-Horowicz, “Identification and mapping of induced chromosomal deletions using sequence polymorphisms.”, BioTechniques, vol. 48 (1) , pp. 53–60, 2010.
  • 2009
    • A. Probst, E. Dunleavy and G. Almouzni, “Epigenetic inheritance during the cell cycle.”, Nat. Rev. Mol. Cell Biol., vol. 10 (3) , pp. 192–206, 2009.
    • A. Poulet, R. Buisson, C. Faivre-Moskalenko, M. Koelblen, S. Amiard, F. Montel, S. Cuesta-Lopez, O. Bornet, F. Guerlesquin, T. Godet, J. Moukhtar, F. Argoul, A. Declais, D. Lilley, S. Ip, S. West, E. Gilson and M. Giraud-Panis, “TRF2 promotes, remodels and protects telomeric Holliday junctions.”, EMBO J., vol. 28 (6) , pp. 641–51, 2009.
    • Y. Barriere, V. Mechin, F. Lafargette, D. Manicacci, F. Guillon, H. Wang, D. Lauressergues, M. Pichon, M. Bosio and C. Tatout, “Towards the discovery of maize cell wall genes involved in silage quality and capacity to biofuel production”, Maydica, pp. 161–198, 2009.
  • 2008
    • E. Vanrobays, A. Leplus, Y. Osheim, A. Beyer, L. Wacheul and D. Lafontaine, “TOR regulates the subcellular distribution of DIM2, a KH domain protein required for cotranscriptional ribosome assembly and pre-40S ribosome export.”, RNA, vol. 14 (10) , pp. 2061–73, 2008.